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Comparative genomics reveals origin of MIR159A–MIR159B paralogy, and complexities of PTGS interaction between miR159 and target GA-MYBs in Brassicaceae

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Abstract

Whole-genome and segmental duplications coupled with sequence and functional diversification are responsible for gene family expansion, and morphological and adaptive diversity. Although broad contours of such processes are understood, detailed investigations on regulatory elements, such as miRNA-transcription factor modules, especially in non-model crop plants with complex genomes, are few. The present study was performed to understand evolutionary history of MIR159 family, and changes in the miRNA-binding site (MBS) of the targets MYB33, MYB65, and MYB101 that may affect post-transcriptional gene silencing. We established orthology and paralogy between members of MIR159 family by reconstructing the phylogeny based on 240 precursor sequences sampled across green plants. An unambiguous paralogous relationship between MIR159A and MIR159B was observed only in Brassicaceae which prompted us to analyze the origin of this paralogy. Comparative micro-synteny of ca. 100 kb genomic segments surrounding MIR159A, MIR159B, and MIR159C loci across 15 genomes of Brassicaceae revealed segmental duplication that occurred in the common ancestor of Brassicaceae to be responsible for origin of MIR159A–MIR159B paralogy; extensive gene loss and rearrangements were also encountered. The impact of polyploidy was revealed when the three sub-genomes—least fractionated (LF), moderately fractionated (MF1), and most fractionated (MF2) sub-genomes of Brassica and Camelina sativa—were analyzed. Extensive gene loss was observed among sub-genomes of Brassica, whereas those in Camelina were largely conserved. Analysis of the target MYBs revealed the complete loss of MYB33 homologs in a Brassica lineage-specific manner. Our findings suggest that mature miR159a/b /c are capable of targeting MYB65 across Brassicaceae, MYB33 in all species except Brassica, and MYB101 only in Arabidopsis thaliana. Comparative analysis of the mature miRNA sequence and the miRNA-binding site (MBS) in MYB33, MYB65, and MYB101 showed the complexity of regulatory network that is dependent on strict sequence complementarity potentially leading to regulatory diversity.

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Funding

The study was supported by a DBT Grant number BT/PR628/AGR/36/674/2011 to SD. Financial assistance in the form of JRF/SRF to SA from DBT and non-NET fellowship to ML from DU/UGC is gratefully acknowledged. SD would also like to acknowledge Delhi University for the financial and infrastructural support through R&D Grants.

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  1. Department of Botany, University of Delhi, Delhi, 110007, India

    Saurabh Anand, Mukund Lal & Sandip Das

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  1. Saurabh Anand
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438_2019_1540_MOESM1_ESM.ai

Reconstruction of phylogenetic relationship among homologs and homeologs of MIR159A, MIR159B and MIR159C across Brassicaceae using GTR and doublet model of Bayesian method. Homologs and homeologs of MIR159A-MIR159B can be observed forming sister clade. Within each branch, genome and sub-genome (LF/MF1/MF2) specific clustering can be observed reflecting that the MIR159A-MIR519B paralogy occurred in the ancestral Brassicaceae and precedes genome duplication. (AI 190 KB)

438_2019_1540_MOESM2_ESM.ai

Micro-synteny analysis across genomic regions (100 kb) flanking MIR159B(A) and MIR159C(B) from different genomes of Brassicaceae showing duplication, losses and rearrangement of Protein coding genes, and MIRNA in A. thaliana and their homologs are represented by different colours, and connected. Genes unique to a particular genomic segment are marked by black arrows. Details of genes in each genome and alphabetical letters marking specific duplications and insertion are discussed in detail in text, and in supplementary table 3 and 4. A: Black square blocks marked as A and B show Capsella grandiflora specific segmental duplication; black oval region show BB genome specific duplication in B. juncea and B. nigra. Rounded rectangle indicates A. thaliana specific gene duplication. (AI 1082 KB)

438_2019_1540_MOESM3_ESM.ai

Graphical representation of percentage conservation of genes predicted by AVID/VISTA and FGENESH analysis in homologous and homeologous genomic segments harbouring MIR159A (A), MIR159B (B) and MIR159C (C) across 14 genomes (A. lyrata, C. rubella, C. sativa, B. rapa, B. oleracea, B. napus, B. juncea, B. nigra, S.irio, T. halophila, T. salsuginea, B. sricta, C. grandiflora, and A. arabicum). (AI 2713 KB)

438_2019_1540_MOESM4_ESM.ai

Graphical representation of gene density (one gene per xx kb) in homologous and homeologous genomic segments harbouring miR159A (A), miR159B (B) and miR159C (C) across 14 genomes (A. lyrata, C. rubella, C. sativa, B.rapa, B. oleracea, B. napus, B. juncea, B. nigra, S. irio, T. halophila, T. salsuginea, B. sricta, C. grandiflora, and A. arabicum). (AI 5031 KB)

438_2019_1540_MOESM5_ESM.ai

Impact of genome fractionation on three sub-genomes (LF, MF1 and MF2) of B. rapa (I), B. oleracea (II), B. napus A (III), B. napus C (IV) and C. sativa (V) harbouring MIR159A. Alphabetical letters represent various genes exhibiting retention and the losses (explained in text, and supplementary tables 5, 6) (AI 1133 KB)

438_2019_1540_MOESM6_ESM.ai

Impact of genome fractionation on three sub-genomes (LF, MF1 and MF2) of B. rapa (I), B. oleracea (II), B. napus A (III), B. napus C (IV) and C. sativa (V) harbouring MIR159B. Alphabetical letters represent various genes exhibiting retention and the losses (explained in text, and supplementary tables 5, 6). (AI 1120 KB)

438_2019_1540_MOESM7_ESM.ai

Impact of genome fractionation on three sub-genomes (LF, MF1 and MF2) of B. rapa (I), B. oleracea (II), B. napus A (III), B. napus C (IV) and C. sativa (V) harbouring MIR159C. Alphabetical letters represent various genes exhibiting retention and the losses (explained in text, and supplementary tables 5, 6). (AI 1242 KB)

438_2019_1540_MOESM8_ESM.ppt

Sequence polymorphism in mature 21-nt miR159A, miR159B and miR159C (A) and miRNA binding site (MBS) in the target transcription factors- MYB33, MYB65 and MYB101 (B) across selected members of Brassicaceae. (PPT 516 KB)

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Anand, S., Lal, M. & Das, S. Comparative genomics reveals origin of MIR159A–MIR159B paralogy, and complexities of PTGS interaction between miR159 and target GA-MYBs in Brassicaceae. Mol Genet Genomics 294, 693–714 (2019). https://doi.org/10.1007/s00438-019-01540-4

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